Cited by 726Cancer Immunotherapy and BiomarkersT-cell and B-cell ImmunologyImmunotherapy and Immune Responses

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Tumor-Specific T Cell Dysfunction Is a Dynamic Antigen-Driven Differentiation Program Initiated Early during Tumorigenesis

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Schietinger, Andrea, Philip, Mary, Krisnawan, Varintra E., Chiu, Edison Y., Delrow, Jeffrey J., Basom, Ryan S., Lauer, Peter, Brockstedt, Dirk G., Knoblaugh, Sue E., Hämmerling, Günter J., Schell, Todd D., Garbi, Natalio, Greenberg, Philip D.·2016·Immunity

DOI 10.1016/j.immuni.2016.07.011PMC PMC5119632

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Abstract

CD8(+) T cells recognizing tumor-specific antigens are detected in cancer patients but are dysfunctional. Here we developed a tamoxifen-inducible liver cancer mouse model with a defined oncogenic driver antigen (SV40 large T-antigen) to follow the activation and differentiation of naive tumor-specific CD8(+) T (TST) cells after tumor initiation. Early during the pre-malignant phase of tumorigenesis, TST cells became dysfunctional, exhibiting phenotypic, functional, and transcriptional features similar to dysfunctional T cells isolated from late-stage human tumors. Thus, T cell dysfunction seen in advanced human cancers may already be established early during tumorigenesis. Although the TST cell dysfunctional state was initially therapeutically reversible, it ultimately evolved into a fixed state. Persistent antigen exposure rather than factors associated with the tumor microenvironment drove dysfunction. Moreover, the TST cell differentiation and dysfunction program exhibited features distinct from T cell exhaustion in chronic infections. Strategies to overcome this antigen-driven, cell-intrinsic dysfunction may be required to improve cancer immunotherapy.

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“…studies have demonstrated that blocking inhibitory receptors (checkpoint blockade) can mediate functional rescue of unresponsive T cells in chronic infection or tumors (Barber et al., 2006; Brahmer et al., 2012; Perez-Gracia et al., 2014; (A) Tamoxifen (Tam)-inducible ASTxCre-ERT2 tumor model.”
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Additional file 11 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 10 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693871
Additional file 15 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 9 of Prognostic value of immune factors in the tumor microenvironment of patients with pancreatic ductal adenocarcinoma
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Additional file 6 of Prognostic value of immune factors in the tumor microenvironment of patients with pancreatic ductal adenocarcinoma
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Additional file 2 of Identification of a Novel CD8+ T cell exhaustion-related gene signature for predicting survival in hepatocellular carcinoma
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Additional file 4 of Prognostic value of immune factors in the tumor microenvironment of patients with pancreatic ductal adenocarcinoma
Kiryu, S., Ito, Z., Suka, M., Bito, T., Kan, S., Uchiyama, K., Saruta, M., Hata, T., Takano, Y., Fujioka, S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16986703
Additional file 1 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693844
Additional file 5 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693856
Additional file 9 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693868
Additional file 3 of Prognostic value of immune factors in the tumor microenvironment of patients with pancreatic ductal adenocarcinoma
Kiryu, S., Ito, Z., Suka, M., Bito, T., Kan, S., Uchiyama, K., Saruta, M., Hata, T., Takano, Y., Fujioka, S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16986697
Additional file 6 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693859
Additional file 3 of Microenvironment characterization and multi-omics signatures related to prognosis and immunotherapy response of hepatocellular carcinoma
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Additional file 12 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693877
Additional file 14 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693883
Additional file 1 of Prognostic value of immune factors in the tumor microenvironment of patients with pancreatic ductal adenocarcinoma
Kiryu, S., Ito, Z., Suka, M., Bito, T., Kan, S., Uchiyama, K., Saruta, M., Hata, T., Takano, Y., Fujioka, S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16986688
Additional file 3 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693850
Additional file 13 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693880
Additional file 1 of Microenvironment characterization and multi-omics signatures related to prognosis and immunotherapy response of hepatocellular carcinoma
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Additional file 7 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693862
Additional file 4 of Identification of a Novel CD8+ T cell exhaustion-related gene signature for predicting survival in hepatocellular carcinoma
Liu, K., Liu, J., Zhang, X., Liu, D., Yao, W., Bu, Y., & Chen, B. (2024) · Figshare · doi:10.6084/m9.figshare.26649102
Additional file 8 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693865
Additional file 2 of Prognostic value of immune factors in the tumor microenvironment of patients with pancreatic ductal adenocarcinoma
Kiryu, S., Ito, Z., Suka, M., Bito, T., Kan, S., Uchiyama, K., Saruta, M., Hata, T., Takano, Y., Fujioka, S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16986694
Additional file 7 of Prognostic value of immune factors in the tumor microenvironment of patients with pancreatic ductal adenocarcinoma
Kiryu, S., Ito, Z., Suka, M., Bito, T., Kan, S., Uchiyama, K., Saruta, M., Hata, T., Takano, Y., Fujioka, S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16986715
Additional file 2 of Immunological and genetic kinetics from diagnosis to clinical progression in chronic lymphocytic leukemia
Jiménez, I., Tazón‐Vega, B., Abrisqueta, P., Nieto, J. C., Bobillo, S., Palacio-Garcia, C., Carabia, J., Valdés‐Mas, R., Munuera, M., Puigdefàbregas, L., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14634084
Additional file 5 of Prognostic value of immune factors in the tumor microenvironment of patients with pancreatic ductal adenocarcinoma
Kiryu, S., Ito, Z., Suka, M., Bito, T., Kan, S., Uchiyama, K., Saruta, M., Hata, T., Takano, Y., Fujioka, S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16986706
Additional file 4 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693853
Additional file 2 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693847
Additional file 3 of Identification of a Novel CD8+ T cell exhaustion-related gene signature for predicting survival in hepatocellular carcinoma
Liu, K., Liu, J., Zhang, X., Liu, D., Yao, W., Bu, Y., & Chen, B. (2024) · Figshare · doi:10.6084/m9.figshare.26649099
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Authors: Schietinger, A., Philip, M., Krisnawan, V. E., Chiu, E. Y., Delrow, J. J., Basom, R. S., Lauer, P., Brockstedt, D. G., Knoblaugh, S. E., Hämmerling, G. J., Schell, T. D., Garbi, N., & Greenberg, P. D.
Affiliations: Memorial Sloan Kettering Cancer Center (US)
University of Washington (US)
Fred Hutch Cancer Center (US)
Aduro BioTech (United States) (US)
German Cancer Research Center (DE)
Pennsylvania State University (US)
University of Bonn (DE)
Corresponding author: Schietinger, Andrea
Greenberg, Philip D.
ORCID: Schietinger, Andrea
Philip, Mary
Chiu, Edison Y.
Delrow, Jeffrey J.
Basom, Ryan S.
Lauer, Peter
Brockstedt, Dirk G.
Knoblaugh, Sue E.
Schell, Todd D.
Garbi, Natalio
Greenberg, Philip D.
Venue: Immunity
Publisher: Elsevier BV
Published: 2016-08
Volume: 45
Issue: 2
Pages: 389-401
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2016.07.011
PMC: PMC5119632
OpenAlex: W2514996992
Cited by: 720
References: 60
Citations by year: 2026: 45 · 2025: 77 · 2024: 93 · 2023: 84 · 2022: 78 · 2021: 103 · 2020: 99 · 2019: 61 · 2018: 50 · 2017: 25 · 2016: 5
FWCI: 25.49
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 380 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R00CA172371, K99CA172371, K08CA158069, R01CA033084, P30CA008748, P30CA015704)
National Institute of Allergy and Infectious Diseases (R21AI107776)
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: tumor-specific T cells, CD8+ T cell dysfunction, carcinogenesis, SV40 large T antigen, liver cancer, T cell differentiation, T cell exhaustion, cancer immunotherapy
MeSH terms: Animals, Antigens, Polyomavirus Transforming, Cell Differentiation, Cells, Cultured, Disease Models, Animal, Humans, Liver Neoplasms, Lymphocyte Activation, Mice, Inbred C57BL, Mice, Transgenic, Tamoxifen, Immunotherapy, Adoptive, Cellular Senescence, CD8-Positive T-Lymphocytes, Cancer Vaccines, Mice, Tumor Microenvironment, Carcinogenesis

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Tumor-Specific T Cell Dysfunction Is a Dynamic Antigen-Driven Differentiation Program Initiated Early during Tumorigenesis

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